Socioeconomic valorization and development of a bio-fungicide from essential oils of four Algerian aromatic and medicinal plants: Artemisia herba alba Asso, Mentha pulegium L, Rosmarinus officinalis L and Ocimum basilicum L.

 

Zineb Mahcene^1*, Zoubida Mahcene², Kamilia Bireche³, Fateh Serdouk⁴

¹Faculty of Natural Sciences and Life Sciences, Department of Biological sciences, Lab of Protecting Ecosystems in Arid and Semi Arid areas., Ouargla 30000, Algeria.

²Faculty of Economics, Commercial Sciences and Management, Department of economic sciences,

Ouargla 30000, Algeria.

³Faculty of Mathematics and Science of Matter, Department of Biological sciences, Lab of Valorization and Promotion of Saharan Resources, Ouargla 30000, Algeria.

⁴Faculty of Economics, Commercial and Management sciences, Department of Chimical Sciences,

El oued 39000, Algeria.

 

ABSTRACT:

This work aims to research new bio-fungicidal molecules based on the essential oils (EO) of Artemisia herba alba Asso, Mentha pulegium L, Rosmarinus officinalis L and Ocimum basilicum L for the food protection and preservation against fungal attacks, also, to determine the chemical composition and the socio-economic interest of oil. The plant material used in this study is represented by the aerial part of O. basilicum L., A. herba-alba Asso, M. pulegium L and the leaves and flowers of R. officinalis L dried for a week, protected from the light and at room temperature. EO chemical composition analysis by GC/MS revealed 36, 26, 34 and 27 constituents for A. herba alba Asso, R. officinalis L, O. basilicum L and M. pulegium L EO, respectively. The antifungal activity of the oils was tested using the direct contact PDA method by determining mycelial growth rate and the minimum inhibitory concentration (MIC). The results of the antifungal study showed that all the fungal strains tested are sensitive to different concentrations of the EO applied with a great antifungal potential by an MIC between 139.08 and 1082.76 µg/ml. Thanks to the antifungal power of the EO of the plants studied, the latter demonstrate that the can constitute an important source of several active ingredients including the antifungal activity necessary for a bio-fungicidal product with a more advantageous national socioeconomic level.

 

 

 

INTRODUCTION:

Plants are potent biochemists and have been components of phytomedicine. Plant based natural constituents can be derived from any part of plant like bark, leaves, flowers, fruits, seed etc.). Medicinal plants are used by 80% of the world population as the only available medicines especially in developing countries. The medicinal value of plant lies in some chemical substances that produce a definite physiological action of which the most important of these bioactive compounds of plants are alkaloids, flavonoids, tannins, phenolic compounds and in particular the essential oils^1;2. Currently, aromatic plants have a considerable advantage thanks to the progressive discovery of the applications of their essential oils in several fields of economic interest. Such as anti-fungal products. And these importance in the conservation and protection of agricultural and food products, and also in the face of very serious risks for consumers of food treated with chemical fungals by toxic residues^3;4;5;6;7. Therefore, the orientation of research towards bioactive molecules enjoying antioxidant and antifungal activities then seems promising, and requires a mutation which will undoubtedly allow an annexation between the sphere of scientific research and technological growth. and the revival of the economically profitable industrial sector in the field of essential oil production ^8;9;10;6;7. Essential oils of herbs and their components, which are products from the secondary metabolism of plants have many applications in ethno-medicine food, flavouring and preservation as well as in the fragrance and pharmaceuticals industries¹¹. The antimicrobial properties of essential oils have been described, and because of the growing demand on antimicrobials for preventing microbial food spoilage and bacterial infections, there is an increasing interest in medicinal plants as an alternative to synthetic preservatives and antibiotics. Many essential oils are already used in the food industry as flavouring agents and some are  known to exert antimicrobial activity ,but the mechanism of action is often not entirely understood^12;13. The uses of essential oils from medicinal and aromatic plants have been known for a long time, and have been addressed by several studies on the biological activity of essential oils, and their fungitoxic, antibacterial, antioxidant, insecticide, herbicide effects^{14;15;16 ;17;13}.

 

For this interest, essential oils (EO) considered as bioactive natural substances occupy a good choice in the discovery of new bio-fungicidal molecules. Included in this general context, this work aimed to evaluate the antifungal activity of the EO of Artemisia herba alba Asso, Rosmarinus officinalis L, Mentha pulegium L and Ocimum basilicum L for the development and socioeconomic enhancement of a bio-fungicide product for the food industry.

 

MATERIALS AND METHODS:

Vegetal material:

The plant material used in the present study is represented by the aerial part of O. basilicum L., A. herba-alba Asso and M. pulegium L and the leaves and flowers of R. officinalis L. dried for a week, protected from light and at room temperature. The plants were harvested in clean areas, far from any pollution impact.

 

Essential oil extraction:

The EO extraction was achieved by hydrodistillation in a Clevenger apparatus where 100g of dry leaves immersed in a 1000 ml flask of water for 3 h. The EO obtained is stored in a refrigerator at 4°C.

 

Gas chromatography-mass spectrometry analysis:

The chemical analysis of EO was performed at the L.G.P (Process Engineering laboratory) in Kasdi Merbah Ouargla University. The gas chromatograph adopted is a Bruker SCION 436 GC, coupled to a mass spectrometer quadrupole ionization voltage of 70 ev. The column that is used is an HP-5MS; 5% Phenyl Methyl Siloxane with a length of 30 m and an internal diameter of 0.25mm. The wire thickness being 0.25mm. The operating conditions are: - The temperature of the injector (split mode 1:50): 250°C - Temperature programming: from 50°C to 280°C at a rate of 5°C/min. - The vector gas used is helium with a flow rate of 1.2 ml/min. The temperatures of the quadrupole source are fixed, respectively, at 250°C and 280°C. Linear retention indices (RI) for all compounds were determined using n-alkanes as standards. Identification of individual compounds was performed by matching their mass spectral fragmentation patterns with corresponding data available (Wiley 275 library (6^th edition)).

 

Evaluation of antifungal activity:

The fungal strains tested: Aspergillus niger 939N et Aspergillus flavus NRRL, Fusarium graminearum (ITEM 6477), Fusarium culmorum (MPVP/71/V), Fusarium sporotrichioides (ITEM 692) which are fungal strains responsible for spoiling food.

 

Preparation of suspensions and pre-culture of fungal strains:

For Fusarium strains: In Petri dishes containing the solid PDA medium a 6mm disc of each fungal strain is placed in the center of each dish and they are incubated until that the mycelial growth reaches the edges of the Petri dishes¹⁹. The Aspergillus spore suspension was prepared by potterizing the culture in 10mL of sterile distilled water according to the M38-P method recommended by the National Committee for Clinical Laboratory Standards (NCCLS)²⁰. The final suspension obtained is spectrophotometrically adjusted to an DO₄₅₀ value of 0.6¹³.

 

Agar dilution method (direct contact):

The evaluation of the EO antifungal activity is adopted by the direct contact method, we follow the protocol described by GOUDJIL M. B et al⁵ and Laxmi Lal Dangi et al¹⁸: where the technique consists in adding the oil at different concentrations to 30ml PDA liquid medium with the addition of tween 20 drops to obtain concentrations of: 0.125, 0.25, 0.5, 0.75, 1 and 1.5%. After shaking the bottles, the mixture (PDA + HE + Tween 20) is poured into the petri dish. The inoculation is done under the hood, by depositing in the center of the petri dish a mycelial disc (6 mm) from the Fusarium and put 1 or 2μL from the Aspergillus suspension. The witnesses (fungal strains + PDA + Tween 20) are produced under the same conditions without EO. These petri dishes are incubated at 25±2°C for 7 days. Mycelial growth measurements are taken after 72 hours of incubation. All the tests are restarted three times.

 

Inhibition rate (TI%):

Calculating the percentage of growth inhibition relative to the control makes it possible to evaluate the effect of oil concentrations on fungal growth. The technique involves measuring the diameters of different fungal colonies after incubation time required¹⁷.

 

TI (%) = 100 × (dC – dE)/dC

 

TI (%) = inhibition rate expressed as a percentage.

dC = Colony diameter in "positive control" boxes.

 

Determination of minimum inhibitory concentrations (MIC):

The MIC corresponds to the lowest concentration from which no fungal growth is observed. At experimental concentrations where no growth or germination is observed, we tested the fungicidal or fungistatic activity.

 

Determination of mycelial growth rate (VC):

According to Mohamed Bilal Goudjil et al ¹⁷, the rate of mycelial growth of each concentration is determined by the formula:

 

              D1      (D2 – D1) +   (D3 – D2)                     (Dn – D_n-1)

    VC = ––– + ––––––––– + ––––––––– + …………––––––––––

            Te1          Te2                  Te3                               Ten

 

D: Diameter of the growing zone of each day. Te: incubation time.

 

Socio-economic development of the EO market:

The data from the statistical analysis of the socio-economic impact, the world market of EO and the Algerian market of EO during the period 2013-2017 has risen.

 

RESULTS AND DISCUSSIONS:

Essential oils analysis:

The oils obtained from the four plants studied have a mobile and limpid liquid appearance, yellow color and a strong odor. The average yield of EO extracted by hydrodistillation from dry plant materials are variable depending on the plant studied. EO yields of O. basilicum L and A. herba alba Ass were determined at a rate of 0.5% and 0.57%, respectively of dry matter basis, these values relatively lower than those of M. pulegium L (1.10%) and R. officinalis L (0.98%).

The chromatographic analysis of A. herba-alba Asso EO has identified 36 compounds (Table 1) whose Thujone (12.63%), Santolina epoxide (7.29%), Camphor (15.49%) and 4,7,7-Trimethylbicyclo [4.1.0] hept-3-en-2 (13.46%), in which these major components. According to the Table (1), the chromatographic analysis of R. officinalis L EO gives 26 components where terpinol (6.43%), L-borneol (7.74%), camphor (15.64%), eucalyptol (25%) and alpha-pinen (7.98%) are the majority components. The analysis of O. basilicum L EO revealed 34 constituents (Table 1) which group together linalool (29.27%), estargole (9%), eucalyptol (13.52%) and cedrelanol (6.83%) as majority components. Finally, according to the chromatographic analysis of the M. pulegium L EO, it was noted that 27 components have been identified (Table 1) including Cyclohexanone, 5-methyl-2- (1-methyleth (29.78%), cis-Dihydrocarvone (5.38%), l-Menthone (22.53%) and eucalyptol (9.57%) are the major components.  The EO’s content revealed variations in the same plant of different geographical origin, and also in different parts of the tree. However, In comparison with the results obtained by Hedi Mighriet al²¹; Elsherbiny A. Elsherbiny et al²²; Mohamed Bilal Goudjil et al⁹; Yann Olivier et al²³; Ayoub AINANE et al²⁴; Zineb mahcene et al²⁵; Faïza Baghloul et al²⁶; Sérgio Macedo Silva et al²⁷; Anis Bertella et al²⁸, on the main constituents of oil’s composition, they noticed considerable differences “chymotyp”. Generally, it is concluded that the variation in the chemical composition of essential oils results from the geographical origin of the plant, the extraction technique, the time of harvest and climatic factors^{25, 17}.

 

Antifungal activity:

Mycelial growth rate:

Figure (1) represents that the highest rate of mycelial growth is recorded at 0% in the absence of EO with a rate of 0.7 mm / h, although, this rate is reduced with the increase of the oils different concentration tested. Strain velocity decreased to complete inhibition (0 mm / hr) at a concentration of 0.25% EO of A. herba alba Asso for, F. sporotrichioides and 0.5% for the other strains (F. culmorum and F. graminearum) and 1.5% for A. niger and A. flavus respectively.  The rate of mycelial growth was reduced to complete inhibition under the influence of O basilicum L EO at 0.25% for Fusarium strains and 0.5% for Aspergillus strains. The effect of R. officinalis L EO on mycelial growth rate decreased until total inhibition to 0.5% for F. graminearum, 0.75% and 1% for F. culmorum and F. sporotrichioides, respectively and of 1.5% and 2% for A. niger and A. flavus; respectively. Finally, the M. pulegium L EO completely inhibited the growth rate of F. graminearum (0.75%), F. sporotrichioides (1%), F. culmorum (1%), A. niger (1.5%) and A. flavus (1.5%).

 

Table 1: Chemical compounds of R. officinalis L, M. pulegium L and O. basilicum L oil's

 

 

Fig. 1: Speed of mycelial growth under the effect of essential oils.

 

Minimum inhibitory concentrations (MIC):

The plant oils exerted a significant inhibitory activity against the strains tested. The diameters, the speed of the growth of mycelium decrease each time the concentration of each EO is increased until the non-germination of the disc at the determined MIC. According to Figure (2) and Table (2), it was noted that all the concentrations of the oils applied partially or completely prevented the fungal strains growth. Indeed, for R. officinalis L EO the MIC are 0.5% (270.69µg/ml) against F. graminearum, 0.75% (406.035µg/ml) against F. culmorum, 1% (541.38µg/ml) against F. sporotrichioides and 1.5% (812.07µg/ml) and 2% (1082.76µg/ml) against A. niger and A. flavus, respectively. MIC values of O. basilicum L EO is 0.25% (139.08µg/ml) for strains of Fusarium and 0.5% (278.16 µg/ml) for strains of Aspargillus. The EO effect of A. herba alba Asso shows an MIC is 0.25% (140.505µg/ ml) against F. sporotrichioides, 0.5% (281.01µg/ml) against the other Fusarium strains tested, 1% (562.02µg /ml) and 1.5 % (843.03µg/ml) against A. flavus and A. niger, respectively. The M. pulegium L EO was given a MIC varied according to the fungal strains tested of such fate of 0.75% (142.11µg/ml) against F. graminearum, of 1% (279.48µg/ml) against F. sporotrichioides and F. culmorum and 1.5% (419.22µg/ml) against A. niger and A. flavus.

 

Table 2: The minimum inhibitory concentration of the oils tested against the strains.

 

Fig. 2: Strain inhibition rate as a function of the concentration of essential oil

 

Overall, through the MIC results obtained from the four oils studied, we can see that the EO of M. pulegium L and O. basilicum L show a stronger antifungal activity thanks to their MIC is lower than 500µg/ml. Also, the R. officinalis L EO shows stronger antifungal activity against strains of Fusarium but moderate activity against A. niger (600 <MIC <1500). In addition, strong antifungal activity was recorded by A. herba alba Asso EO against all strains tested except the A. niger strain which EO gives moderate activity against it. We have also noticed from Figure (2) that the fungal strains tested are developed after having been stopped by the presence of EO and that its action against the strains is then: Fungicidal effect, against the Fusarium strains at a maximum concentration of 0.5% for the O. basilicum L EO, 0.75% of A. herba alba Asso EO and at a concentration of 2% for R. officinalis. Fungistatic effect, against the two strains of Aspergillus at a concentration of 0.75% for the O. basilicum L EO, 1.5% for the A. herba alba Asso EO and at a concentration of 2% for R. officinalis. Thanks to the results obtained by the study of speed of mycelial growth and the determination of the minimum fungistatic or fungicidal concentration of EO, allow us to say that the four oils reacted positively against the fungal strains. tested. As we notice that the speed of mycelial growth decrease with time under the effect of the low concentration of oils.

 

The detection of the antifungal effect of EO of R. officinalis against the fungal strain A. Niger by Faïza Baghloul et al²⁶, declared that the tested colonies of A. niger showed very low growth at 0.25% EO concentration. From a concentration of 0.5%, it noticed a total absence of growth that these results are more important to ours. In addition, the results of the study of the antifungal potency of A. herba alba Asso by Goudjil M. Bilal et al⁹ show an MIC is 0.5% for strains of F. moniliforme with a fungicidal effect and F. oxysporum with a fungistatic effect. For S. solani and F. solani, the MIC is around 0.75%. The MIC detection of pennyroyal by D. Ouraini et al²⁹, states that this oil affects all dermatophytes with an MIC corresponds to 10%. Shama Hmiri et al³⁰, show that the M. pulegium EO exerted a remarkable inhibitory activity on the three molds A. alternata, B. cinerea and P. expansum with MIC of 156 and 300μl/l, respectively. The results obtained by Koffi Apeti Gbogbo et al³¹ on the antifungal activity of O. basilicum L EO on micromycetes influencing the germination of Maize and Cowpea, show that the development of Nigrospora oryzae and Alternaria alternata is not affected by the low amounts (0.07, 0.142 and 0.285μl/ml) of O. basilicum EO, on the other hand, at the highest concentration (1.l4μl/ml), the weakest effect is obtained on Nigrospora oryzae. This results in an inhibition of thallus development of 86%. The other strains have inhibitions varying from 94% to 100%. Nidhi Rao et al³² found that the antifungal activity of Curcuma longa was positive against Candida albicans (13 mm) and no activity was shown against Aspergillus flavus, Aspergillus niger and Aspergillus fumigates.

 

The difficulty of developing an antifungal molecule is linked to the ultrastructure of the fungal cell which presents three barriers: the cell wall, chitin, membrane ergosterol and the eukaryotic nucleus; and second, the antifungal molecules themselves can lead to resistance⁵. In fact, the active components attack the cell wall and membrane, thereby affecting the permeability and release of intracellular constituents, also interfering with the function of the membrane^25;26. According to the observations of Soylu et al³³, EO can alter the morphology of thalli they cause large vesicles to appear inside the cell wall. In many cases, the cells of the mycelium no longer have a cytoplasm or cytoplasm depleted of organelles. Similar observations with other EO have been reported by Zambonelli et al³⁴; Fiori A.C.G et al³⁵; Degryse Anne-Claire et al³⁶, observed that EO act in a targeted manner on the sporulation phase. This effect may be linked to a longer vulnerable period, which facilitates the penetration of EO into the cell. In addition, Carmo E.S et al³⁷; Jiali Dai et al⁴, report that EO damage a series of enzyme systems in molds, affecting the synthesis and production of structural component energy, which enter into the composition of the cell wall, which disrupts fungal growth. These suggestions have already been reported by Bang K.H et al ³⁸, studied the inhibition of enzymes synthesizing the wall of fungal cells by examining the inhibitory effects of EO on β- (1.3) glucan on chitin synthase.

 

Moreover, Ferdeş M, C. Ungureanu³⁹; Mallappa Kumara Swamy et al⁴⁰, confirmed that the EO of aromatic plants such as lemon, mint, juniper, basil, citrus, fennel, oregano, rosemary and thyme have considerable antifungal activity against a wide range of fungal pathogens such as strains of Aspergillus niger, Fusarium oxysporum, Monascus purpureus and Penicillium hirsutum. According to Pattnaik. S et al⁴¹ and Laib Imène⁴², the antifungal activity of an EO is to be demonstrated with its chemical composition, the functional groups of the majority compounds (alcohols, phenols, terpene and ketone compounds) and the possible synergistic effects between components. Thus, the nature of the chemical structures which constitute it, but also their proportions play a determining role. However, it is likely that the minority components act synergistically^36;10. According to Shama Hmiri et al⁴³, The antimicrobial activity of M. pulegium oil could be attributed to its major compounds, which are oxygenated monocyclic monoterpenes. Naouel, K et al⁴⁴ studied the inhibitory effect of A. herba alba Asso EO on two strains of Fusarium oxysporum, the results showed that the antifungal activity is mainly due to substances contained in the extracts of the plant's EO. In their study on the antifungal effect of EO, Laib Imène⁴²; Tabassum Nuzhat and Vidyasagar. G. M⁴⁵, reported that the major components of the EO of R. officinalis (α-pinene, borneol, camphene, camphor, verbenone and bornyl acetate) have an inhibitory effect on fungal growth especially on species of the genus Fusarium. This antifungal activity can be explained by the fact that it is a chemotype, pulégone, menthone, menthol and carvone, which exert a total inhibition of germination also have a moderate effect on micromycetes^43;46;9.

The mechanism of action of terpenes is not fully understood, but it is likely that these lipophilic compounds cause a loss of membrane integrity in fungi. On the other hand, the mechanism of phenolic toxicity on fungi is mainly based on the inhibition of fungal enzymes containing the SH fragment in their active site ^{46; 17}.

 

Morphological changes (color of mycelium, mycelial tears, etc.) were observed on the effect of deferent concentrations of EO. Sharma. N and Tripath. A⁴³, found that EO can cause pigmentation loss for molds on the one hand. On the other hand, Salhi. N et al⁴⁷ reported that loss or change in color for the genus Fusarium may be correlated with loss of mycotoxin production.

 

Socio-economic development of the EO market:

Currently, EO from aromatic plants have a considerable advantage thanks to the gradual discovery of applications in several areas of economic interest. Their numerous uses mean that they are experiencing increasing demand on world markets. The aromatic and medicinal plants, opens new perspectives in different economic sectors via the economic valuation of the products of EO. Although The market for new organic industries, such as bio-fungicides, is still little exploited at global and national level, and characterized by the lack of detailed, reliable and precise information^48;49. For that they are valued economically through the market of essential oils included in this industry. Therefore, we will adopt the Economic valuation of the essential oils market in Algeria, as main indicator for the economic valuation of EO products.

 

 

Fig. 3:  List of supplying markets for a product imported by Algeria

 

Product: 3301 Essential oils, whether or not terpeneless, incl. concretes and absolutes; resinoids; extracted oleoresins; concentrates of essential oils in fats, fixed oils, waxes or the like, obtained by enfleurage or maceration; terpenic by-products of the deterpenation of essential oils; aqueous distillates and aqueous solutions of essential oils. Sources: ITC (2018) calculations based on UN COMTRADE statistics. http://comtrade.un.org/.

 

Socio-economic impact:

The Floristic Potentialities in Algeria is of a very diversified flora as a consequence of the geographical situation of Algeria, overlapping between two floral empires: Holarctis and Paleotropis, including 3139 species⁴³. Among these species, 551 are protected by law Executive Decree⁵⁰. The flora species in Algeria are classified according to their degree of rarity: 289 fairly rare species, 647 rare species, 640 very rare species, 35 extremely rare species and 168 endemic species⁵¹. There is also reason to articulate that its outcome on the national socioeconomic level is presented by the development potential of this sector in terms of the advantage of being a job-creating activity, an activity also which generates profitable income from local populations and finally an activity with high added value which makes it possible to develop niche markets, and to contribute to diversification and national economic development⁵².

The world and Algerian essential oils market:

The world market of essential oils, is estimated at more than 5.5 billion dollars in 2017⁴⁷. With à trade balance of 17 451 thousand USD in 2017. Imports and exports of essential oils increase regularly throughout the period. With an annual growth rate in value between 2013-2017 of 8%, for imports, and 7% for exports. Algerian imports in EO reported an increase of 20% in volume and more than 16% in value of imports in HE compared to the year 2013. Algeria imported for 9019 thousand USD at the end of the year 2014 against 5275 thousand USD in the same period of comparison with the year 2013. The trade balance is negative of -8 994 thousand USD in 2017. Conversely, imports are increasing (Fig. 3)⁵³.

 

According to Figure (3), The main suppliers of EO for Algeria for 2013 to 2017 are (France, Italy, Spain, Turkey and China). For the year 2017, the growth of imports of Algeria in essential oils record 17%, which is higher than that of world exports by 7%.

 

According to Figure (4), the main importing markets for a product exported by Algeria for 2013 to 2017 are (Tunisia, Spain, Mauritania, Canada and United Kingdom). For the year 2017, the total exported value to the world is 25 thousand USD.

 

 

Fig. 4: List of importing markets for a product exported by Algeria

 

Product: 3301 Essential oils, whether or not terpeneless, incl. concretes and absolutes; resinoids; extracted oleoresins; concentrates of essential oils in fats, fixed oils, waxes or the like, obtained by enfleurage or maceration; terpenic by-products of the deterpenation of essential oils; aqueous distillates and aqueous solutions of essential oils. Sources: ITC (2018) calculations based on UN COMTRADE statistics. http://comtrade.un.org/.

 

CONCLUSION:

The study of the antifungal activity shows that the EO of the four plants presented in this study show a broad spectrum of action on the fungal strains tested. Indeed, O. basilicum L, M. pulegium L and A. herba alba Asso has very pronounced antifungal properties on the strains tested. On the other hand, the EO of R. officinalis L was found to be less active. These EO can therefore constitute a credible bio-fungicide product in the fungicides market for the food industry. In addition to meeting national demand, as soon as Algeria is declared a net importing country of EO. With the export expectations, in view of the non-exploited floristic potentials in Algeria, In addition, given the increase in the growth of world demand for EO products.

 

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Received on 12.08.2020                    Modified on 05.09.2020

Accepted on 27.09.2020                   ©AJRC All right reserved